More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance

Nature Cell Biology

Volumn 13, Issue 10, 2011, Pages 1161-1169

  Lukas, Jiri ^a   Lukas, Claudia ^a   Bartek, Jiri ^a,b  

^a DANISH CANCER SOCIETY RESEARCH CENTER   (Denmark)

^b PALACKÝ UNIVERSITY   (Czech Republic)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2;

ADENOSINE DIPHOSPHATE RIBOSYLATION; CELL FUNCTION; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA STRAND BREAKAGE; DOUBLE STRANDED DNA BREAK; GENOTOXICITY; HISTONE ACETYLATION; HISTONE METHYLATION; HISTONE MODIFICATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPHOSPHORYLATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; REVIEW; SEQUENCE HOMOLOGY; SUMOYLATION; UBIQUITINATION; VDJ EXON;

ANIMALS; CELL CYCLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA DAMAGE; DNA REPAIR; GENOMIC INSTABILITY; HISTONES; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 80053555789     PISSN: 14657392     EISSN: 14764679     Source Type: Journal    
DOI: 10.1038/ncb2344     Document Type: Review

References (102)

1. Rogakou, E. P., Pilch, D. R., Orr, A. H., Ivanova, V. S. & Bonner, W. M. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J. Biol. Chem. 273, 5858-5868 (1998). (Pubitemid 28124064)
2. Ciccia, A. & Elledge, S. J. The DNA damage response: making it safe to play with knives. Mol. Cell 40, 179-204 (2010).
3. Polo, S. E. & Jackson, S. P. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 25, 409-433 (2011).
4. Krishnakumar, R. & Kraus, W. L. The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol. Cell 39, 8-24 (2010).
5. Messner, S. et al. PARP1 ADP-ribosylates lysine residues of the core histone tails. Nucleic Acids Res. 38, 6350-6362 (2010).
6. Polo, S. E., Kaidi, A., Baskcomb, L., Galanty, Y. & Jackson, S. P. Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J. 29, 3130-3139 (2010).
7. Chou, D. M. et al. A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc. Natl Acad. Sci. USA 107, 18475-18480 (2010).
8. Facchino, S., Abdouh, M., Chatoo, W. & Bernier, G. BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery. J. Neurosci. 30, 10096-10111 (2010).
9. Ismail, I. H., Andrin, C., McDonald, D. & Hendzel, M. J. BMI1-mediated histone ubiquitylation promotes DNA double-strand break repair. J. Cell Biol. 191, 45-60 (2010).
10. Larsen, D. H. et al. The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage. J. Cell Biol. 190, 731-740 (2010).
11. Smeenk, G. et al. The NuRD chromatin-remodeling complex regulates signaling and repair of DNA damage. J. Cell Biol. 190, 741-749 (2010).
12. Bekker-Jensen, S. et al. Human Xip1 (C2orf13) is a novel regulator of cellular responses to DNA strand breaks. J. Biol. Chem. 282, 19638-19643 (2007). (Pubitemid 47100052)
13. Iles, N., Rulten, S., El-Khamisy, S. F. & Caldecott, K. W. APLF (C2orf13) is a novel human protein involved in the cellular response to chromosomal DNA strand breaks. Mol. Cell Biol. 27, 3793-3803 (2007). (Pubitemid 46726186)
14. Kanno, S. et al. A novel human AP endonuclease with conserved zinc-finger-like motifs involved in DNA strand break responses. EMBO J. 26, 2094-2103 (2007). (Pubitemid 46625798)
15. Rulten, S. L. et al. PARP-3 and APLF function together to accelerate nonhomologous end-joining. Mol. Cell. 41, 33-45 (2011).
16. Ahel, I. et al. Poly(ADP-ribose)-binding zinc finger motifs in DNA repair/checkpoint proteins. Nature 451, 81-85 (2008).
17. Mehrotra, P. V. et al. DNA repair factor APLF is a histone chaperone. Mol. Cell 41, 46-55 (2011).
18. Ahel, D. et al. Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 325, 1240-1243 (2009).
19. Gottschalk, A. J. et al. Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc. Natl Acad. Sci. USA 106, 13770-13774 (2009).
20. Xiao, A. et al. WSTF regulates the H2A.X DNA damage response via a novel tyrosine kinase activity. Nature 457, 57-62 (2009).
21. Cook, P. J. et al. Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions. Nature 458, 591-596 (2009).
22. Jungmichel, S. & Stucki, M. MDC1: The art of keeping things in focus. Chromosoma 119, 337-349 (2010).
23. Wang, J., Gong, Z. & Chen, J. MDC1 collaborates with TopBP1 in DNA replication checkpoint control. J. Cell Biol. 193, 267-273 (2011).
24. Ichijima, Y. et al. MDC1 directs chromosome-wide silencing of the sex chromosomes in male germ cells. Genes Dev. 25, 959-971 (2011).
25. Berkovich, E., Monnat, R. J., Jr. & Kastan, M. B. Roles of ATM and NBS1 in chromatin structure modulation and DNA double-strand break repair. Nat. Cell Biol. 9, 683-690 (2007). (Pubitemid 47214731)
26. Savic, V. et al. Formation of dynamic γ-H2AX domains along broken DNA strands is distinctly regulated by ATM and MDC1 and dependent upon H2AX densities in chromatin. Mol. Cell 34, 298-310 (2009).
27. Iacovoni, J. S. et al. High-resolution profiling of γH2AX around DNA double strand breaks in the mammalian genome. EMBO J. 29, 1446-1457 (2010).
28. Kim, J. A., Kruhlak, M., Dotiwala, F., Nussenzweig, A. & Haber, J. E. Heterochromatin is refractory to γ-H2AX modification in yeast and mammals. J. Cell Biol. 178, 209-218 (2007). (Pubitemid 47076458)
29. Wood, J. L., Singh, N., Mer, G. & Chen, J. MCPH1 functions in an H2AX-dependent but MDC1-independent pathway in response to DNA damage. J. Biol. Chem. 282, 35416-35423 (2007). (Pubitemid 350232410)
30. Peng, G. et al. BRIT1/MCPH1 links chromatin remodelling to DNA damage response. Nat. Cell Biol. 11, 865-872 (2009).
31. Moon, S. H., Nguyen, T. A., Darlington, Y., Lu, X. & Donehower, L. A. Dephosphorylation of γ-H2AX by WIP1: an important homeostatic regulatory event in DNA repair and cell cycle control. Cell Cycle 9, 2092-2096 (2010).
32. Xu, Y. & Price, B. D. Chromatin dynamics and the repair of DNA double strand breaks. Cell Cycle 10, 261-267 (2011).
33. Sun, Y. et al. Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60. Nat. Cell Biol. 11, 1376-1382 (2009).
34. Ayoub, N., Jeyasekharan, A. D., Bernal, J. A. & Venkitaraman, A. R. HP1-β mobilization promotes chromatin changes that initiate the DNA damage response. Nature 453, 682-686 (2008). (Pubitemid 351769293)
35. Luijsterburg, M. S. et al. Heterochromatin protein 1 is recruited to various types of DNA damage. J. Cell Biol. 185, 577-586 (2009).
36. Baldeyron, C., Soria, G., Roche, D., Cook, A. J. & Almouzni, G. HP1α recruitment to DNA damage by p150CAF-1 promotes homologous recombination repair. J. Cell Biol. 193, 81-95 (2011).
37. Xu, Y. et al. The p400 ATPase regulates nucleosome stability and chromatin ubiquitination during DNA repair. J. Cell Biol. 191, 31-43 (2010).
38. Miller, K. M. et al. Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat. Struct. Mol. Biol. 17, 1144-1151 (2010).
39. Soutoglou, E. et al. Positional stability of single double-strand breaks in mammalian cells. Nat. Cell Biol. 9, 675-682 (2007). (Pubitemid 47214730)
40. Doil, C. et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136, 435-446 (2009).
41. Stewart, G. S. et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 136, 420-434 (2009).
42. Bekker-Jensen, S. & Mailand, N. The ubiquitin-and SUMO-dependent signaling response to DNA double-strand breaks. FEBS Lett. http://dx.doi.org/10. 1016/j. febslet.2011.05.056 (2011).
43. Huen, M. S. et al. Regulation of chromatin architecture by the PWWP domain-containing DNA damage-responsive factor EXPAND1/MUM1. Mol. Cell 37, 854-864 (2010).
44. Cescutti, R., Negrini, S., Kohzaki, M. & Halazonetis, T. D. TopBP1 functions with 53BP1 in the G1 DNA damage checkpoint. EMBO J. 29, 3723-3732 (2010).
45. Watanabe, K. et al. RAD18 promotes DNA double-strand break repair during G1 phase through chromatin retention of 53BP1. Nucleic Acids Res. 37, 2176-2193 (2009).
46. Huang, J. et al. RAD18 transmits DNA damage signalling to elicit homologous recombination repair. Nat. Cell Biol. 11, 592-603 (2009).
47. Bekker-Jensen, S. et al. HERC2 coordinates ubiquitin-dependent assembly of DNA repair factors on damaged chromosomes. Nat. Cell Biol. 12, 80-86 (2010).
48. Wu, J. et al. Histone ubiquitination associates with BRCA1-dependent DNA damage response. Mol. Cell Biol. 29, 849-860 (2009).
49. Chernikova, S. B., Dorth, J. A., Razorenova, O. V., Game, J. C. & Brown, J. M. Deficiency in Bre1 impairs homologous recombination repair and cell cycle checkpoint response to radiation damage in mammalian cells. Radiat. Res. 174, 558-565 (2010).
50. Nakamura, K. et al. Regulation of homologous recombination by RNF20-dependent H2B ubiquitination. Mol. Cell 41, 515-528 (2011).
51. Moyal, L. et al. Requirement of ATM-dependent monoubiquitylation of histone H2B for timely repair of DNA double-strand breaks. Mol. Cell 41, 529-542 (2011).
52. Wu, J. et al. Chfr and RNF8 synergistically regulate ATM activation. Nat. Struct. Mol. Biol. 18, 761-768 (2011).
53. Ikura, T. et al. DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol. Cell Biol. 27, 7028-7040 (2007). (Pubitemid 47549742)
54. Bohgaki, T. et al. Genomic instability, defective spermatogenesis, immunodeficiency, and cancer in a mouse model of the RIDDLE syndrome. PLoS Genet. 7, e1001381 (2011).
55. Bothmer, A. et al. Regulation of DNA end joining, resection, and immunoglobulin class switch recombination by 53BP1. Mol. Cell 42, 319-329 (2011).
56. Shao, G. et al. The Rap80-BRCC36 de-ubiquitinating enzyme complex antagonizes RNF8-Ubc13-dependent ubiquitination events at DNA double strand breaks. Proc. Natl Acad. Sci. USA 106, 3166-3171 (2009).
57. Nakada, S. et al. Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature 466, 941-946 (2010).
58. Galanty, Y. et al. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462, 935-939 (2009).
59. Morris, J. R. et al. The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 462, 886-890 (2009).
60. Peuscher, M. H. & Jacobs, J. L. DNA damage response and repair activities at uncapped telomeres depend on RNF8. Nat. Cell Biol. 13,1139-1145 (2011).
61. Huyen, Y. et al. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432, 406-411 (2004). (Pubitemid 39551676)
62. Botuyan, M. V. et al. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127, 1361-1373 (2006). (Pubitemid 44960409)
63. Pei, H. et al. MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites. Nature 470, 124-128 (2011).
64. Hajdu, I., Ciccia, A., Lewis, S. M. & Elledge, S. J. Wolf-Hirschhorn syndrome candidate 1 is involved in the cellular response to DNA damage. Proc. Natl Acad. Sci. USA 108, 13130-13134 (2011).
65. Matsuoka, S. et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316, 1160-1166 (2007). (Pubitemid 46877472)
66. Oda, H. et al. Regulation of the histone H4 monomethylase PR-Set7 by CRL4(Cdt2)-mediated PCNA-dependent degradation during DNA damage. Mol. Cell 40, 364-376 (2010).
67. Yan, Q. et al. BBAP monoubiquitylates histone H4 at lysine 91 and selectively modulates the DNA damage response. Mol. Cell 36, 110-120 (2009).
68. Murga, M. et al. Global chromatin compaction limits the strength of the DNA damage response. J. Cell Biol. 178, 1101-1108 (2007). (Pubitemid 47480219)
69. Bao, S. et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444, 756-760 (2006). (Pubitemid 44949604)
70. Goodarzi, A. A., Jeggo, P. & Lobrich, M. The influence of heterochromatin on DNA double strand break repair: Getting the strong, silent type to relax. DNA Repair (Amst.) 9, 1273-1282 (2010).
71. Goodarzi, A. A., Kurka, T. & Jeggo, P. A. KAP-1 phosphorylation regulates CHD3 nucleosome remodeling during the DNA double-strand break response. Nat. Struct. Mol. Biol. 18, 831-839 (2011).
72. Chiolo, I. et al. Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144, 732-744 (2011).
73. Torres-Rosell, J. et al. The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat. Cell Biol. 9, 923-931 (2007). (Pubitemid 47190447)
74. Dinant, C. et al. Assembly of multiprotein complexes that control genome function. J. Cell Biol. 185, 21-26 (2009).
75. Groth, A., Rocha, W., Verreault, A. & Almouzni, G. Chromatin challenges during DNA replication and repair. Cell 128, 721-733 (2007). (Pubitemid 46273574)
76. Bergink, S. et al. DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev. 20, 1343-1352 (2006). (Pubitemid 43727594)
77. Shanbhag, N. M., Rafalska-Metcalf, I. U., Balane-Bolivar, C., Janicki, S. M. & Greenberg, R. A. ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 141, 970-981 (2010).
78. Lilley, C. E. et al. A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses. EMBO J. 29, 943-955 (2010).
79. Bermejo, R. et al. Genome-organizing factors Top2 and Hmo1 prevent chromosome fragility at sites of S phase transcription. Cell 138, 870-884 (2009).
80. Harrigan, J. A. et al. Replication stress induces 53BP1-containing OPT domains in G1 cells. J. Cell Biol. 193, 97-108 (2011).
81. Lukas, C. et al. 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat. Cell Biol. 13, 243-253 (2011).
82. Letessier, A. et al. Cell-type-specific replication initiation programs set fragility of the FRA3B fragile site. Nature 470, 120-123 (2011).
83. Chan, K. L., Palmai-Pallag, T., Ying, S. & Hickson, I. D. Replication stress induces sister-chromatid bridging at fragile site loci in mitosis. Nat. Cell Biol. 11, 753-760 (2009).
84. Lazzaro, F. et al. Histone methyltransferase Dot1 and Rad9 inhibit single-stranded DNA accumulation at DSBs and uncapped telomeres. EMBO J. 27, 1502-1512 (2008). (Pubitemid 351733336)
85. Yun, M. H. & Hiom, K. CtIP-BRCA1 modulates the choice of DNA double-strand-break repair pathway throughout the cell cycle. Nature 459, 460-463 (2009).
86. Helmink, B. A. et al. H2AX prevents CtIP-mediated DNA end resection and aberrant repair in G1-phase lymphocytes. Nature 469, 245-249 (2011).
87. Zha, S. et al. ATM damage response and XLF repair factor are functionally redundant in joining DNA breaks. Nature 469, 250-254 (2011).
88. Bothmer, A. et al. 53BP1 regulates DNA resection and the choice between classical and alternative end joining during class switch recombination. J. Exp. Med. 207, 855-865 (2010).
89. Cao, L. et al. A selective requirement for 53BP1 in the biological response to genomic instability induced by Brca1 deficiency. Mol. Cell 35, 534-541 (2009).
90. Bouwman, P. et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat. Struct. Mol. Biol. 17, 688-695 (2010).
91. Bunting, S. F. et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141, 243-254 (2010).
92. Coleman, K. A. & Greenberg, R. A. The BRCA1-RAP80 complex regulates DNA repair mechanism utilization by restricting end resection. J. Biol. Chem. 286, 13669-13680 (2011).
93. Hu, Y. et al. RAP80-directed tuning of BRCA1 homologous recombination function at ionizing radiation-induced nuclear foci. Genes Dev. 25, 685-700 (2011).
94. Fong, P. C. et al. Inhibition of poly(ADP-ribose) polymerase in tumors from BRCA mutation carriers. N. Engl. J. Med. 361, 123-134 (2009).
95. Filion, G. J. et al. Systematic protein location mapping reveals five principal chromatin types in Drosophila cells. Cell 143, 212-224 (2010).
96. Schermelleh, L., Heintzmann, R. & Leonhardt, H. A guide to super-resolution fluorescence microscopy. J. Cell Biol. 190, 165-175 (2010).
97. Fierz, B. et al. Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat. Chem. Biol. 7, 113-119 (2011).
98. Jasencakova, Z. et al. Replication stress interferes with histone recycling and predeposition marking of new histones. Mol. Cell 37, 736-743 (2010).
99. Sarkies, P., Reams, C., Simpson, L. J. & Sale, J. E. Epigenetic instability due to defective replication of structured DNA. Mol. Cell 40, 703-713 (2010).
100. O'Hagan, H. M., Mohammad, H. P. & Baylin, S. B. Double strand breaks can initiate gene silencing and SIRT1-dependent onset of DNA methylation in an exogenous promoter CpG island. PLoS Genet. 4, e1000155 (2008).
101. Cuozzo, C. et al. DNA damage, homology-directed repair, and DNA methylation. PLoS Genet. 3, e110 (2007).
102. Devgan, S. S. et al. Homozygous deficiency of ubiquitin-ligase ring-finger protein RNF168 mimics the radiosensitivity syndrome of ataxia-telegiectasia. Cell Death Diff. 18, 1500-1506 (2011).